FOCUS OF FLIES FACILITY RESEARCH: Animal carcasses represent nutrient rich resources, or food-falls, for many organisms ranging from microbes to vertebrate scavengers. Microbes were initially thought of only as nutrient recyclers1. However, Jenzen2 suspected that microbes were competitors with other consumers including insects for these resources. Microbes may alter food resources and produce toxins that affect the “appeal” of the resources, and themselves, to other consumers. Microbes colonizing fish carrion in tidal estuaries will compete with other consumers for these resources3. These microbes release noxious chemicals that deterred consumption of the fish remains by higher level consumers, such as crustaceans3.
Higher order scavengers are selected to have mechanisms countering competition strategies used by microbes also colonizing food-falls. These responses could be behavioral4 or physiological5,6. The burying beetle Nicrophorus vespilloides (Coleoptera: Silphidae), which depends on small carrion as a breeding site, have evolved counterstrategies to suppress microbial communities in order to reduce competition for these resources6. In turn, the presence of some microbes was detrimental to immature development and reproductive success of the burying beetle6. The blow fly Lucilia sericata (Diptera: Calliphoridae) in many instances will colonize and feed on necrotic tissue in wounds on living individuals, and their salivary excretions have antimicrobial activity against Staphylococcus aureus, Streptococcus A and B, as well as Pseudomonas sp7. Similarly, house fly, Musca domestica (Diptera: Muscidae), larvae in target food-falls reduce the growth of competing fungi4. However, interactions between fly and microbe species can be quite diverse depending on the parties involved. In some cases, these interactions are beneficial while in others they are detrimental depending on parameters, such as the microbe and fly species or strains involved, population density, and genetic diversity.
Many saprophagous insects feed directly on microbes associated with decomposing material as part of their diet. House fly larval development is dependent upon bacteria associated with the larval resource8. Black soldier fly, Hermetia illucens (Diptera: Stratiomyidae), which is another colonizer of carrion, can reduce carcass E. coli counts by a log of four9. We determined that black soldier fly larvae reared in dairy manure for 72 hr reduced E. coli by a log of eight10, and it is hypothesized that the bacteria serve as nutrients for larval development.
Competition between microbes and insects for ephemeral resources has resulted in selection towards coexistence11,12 as well as symbiosis13. Such interactions are common in the insect world. Volatiles emitted by microbes, proliferating on decomposing remains14, are used by blow flies to locate these resources15. Bovine blood inoculated with bacteria isolated from wounds infested with Cochliomyia hominivorax (Diptera: Calliphoridae) release volatiles that attract intraspecific adults16. House fly eggs, when deposited, are coated with microbes which potentially produce defensive compounds which offer protection from predators and pathogens13. Once deposited, house flies respond to volatiles emitted by these microbes4. Volatile concentrations below a specific threshold attract individuals that will oviposit, while concentrations above the threshold repel these same individuals4. In addition, volatile concentration positively correlated with microbial population density. Colonization attempts when volatiles were above a noted threshold resulted in reduced survivorship of these eggs to the adult stage, while the opposite was determined for eggs deposited when volatiles were below the identified threshold4. Many microbes, both pathogenic and non-pathogenic, are ingested by developing house flies17, and larvae surviving to the adult stage are inoculated with these microbes which are then dispersed to other resources during subsequent fly oviposition4. In some instances, individuals consuming microbes receive nutritional benefits, such as essential amino acids and vitamins. Tsetse flies, Glossina sp., are provided B vitamins by Wigglesworthia13. Furthermore, Buchnera aphidicola, which is an endosymbiont of aphids, provides essential amino acids to their hosts13.
Blow flies and microbes occurring on food-falls have evolved a mutualistic relationship. Microbes consumed by immature blow flies feeding on a resource18, survive larval molting and pupation, and are present in emergent adult insects which serve as a dispersal mechanism18. The microbes release volatiles that attract blow flies to resources and resulting progeny disperse microbes to new habitats8. However, consumption by the wrong saprophage results in microbial mortality8. We hypothesize that while one bacterial species survives digestion and pupation with one fly species, it will not with another fly species. Therefore, bacterial proliferation and dispersal is mitigated by colonization patterns of fly species. However, such an association could prove detrimental to both species as the volatiles emitted could also attract predators19, such as Chrysomya rufifacies (Diptera: Calliphoridae), to their prey, which would be Cochliomyia macellaria (Diptera: Calliphoridae) larvae in this case.
8. Zurek, L., Schal, C. & Watson, D.W. Diversity and contribution of the intestinal bacterial community to the development of Musca domestica (Diptera: Muscidae) larvae. Journal of Medical Entomology 37, 924-928 (2000).
9. Erickson, M.C., Islam, M., Sheppard, C., Liao, J. & Doyle, M.P. Reduction of Escherichia coli O157:H7 and Salmonella enterica Serovar enteritidis in chicken manure by larvae of the black soldier fly. Journal of Food Protection 67, 685-690 (2004).
10. Liu, Q., Tomberlin, J.K., Brady, J.A., Sanford, M.R. & Yu, Z. Black soldier fly (Diptera: Stratiomyidae) larvae reduce Escherichia coli in dairy manure. Environmental Entomology 37, 1525-1530 (2008).
11. Dale, C., Young, S.A., Haydon, D.T. & Welburn, S.C. The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc. Natl. Acad. Sci. USA 98, 1883-1888 (2001).
16. Chaudhury, M.F., Welch, J.B. & Alvarez, L.A. Response of fertile and sterile screwworm (Diptera: Calliphoridae) flies to bovine blood inoculated with bacteria originating from screwworm infested animal wounds. Journal of Medical Entomology 39, 130-134 (2002).
19. Thomas, R.S., Glen, D.M. & Symondson, W.O.C. Prey detection through olfaction by the soil-dwelling larvae of the carabid predator Pterostichus melanarius. Soil Biology and Biochemistry 40, 207-216 (2008).